Loss of LEFKOTHEA Leads to Global Transcriptional and Post-Transcriptional Changes in Gene Expression During Early Light Response.

In plants, the transition from heterotrophic to autotrophic growth is a critical developmental shift, tightly coupled to the establishment of photosynthesis. This process demands a precise interplay between the nucleus and chloroplasts, with communication schemes providing essential checkpoints to synchronize gene expression during seedling greening and establishment. While light response and photomorphogenesis are known to rely on transcriptional networks, recent evidence highlights a key role for alternative pre-mRNA splicing in facilitating plant adaptation to new light regimes, thereby enhancing transcriptome diversity. LEFKOTHEA, a dual-localized nuclear and chloroplast protein, has emerged as a potential integrator of these processes; it mediates the splicing of both chloroplast group II introns and nuclear introns via interactions with spliceosomal proteins. Here, we demonstrate that LEFKOTHEA is an active component of early light response signaling, regulating gene expression both transcriptionally and post-transcriptionally. Transcriptomic analysis reveals that LEFKOTHEA shapes the transcriptome both quantitatively and qualitatively by modulating alternative splicing, a mechanism essential for plant plasticity and adaptation. Furthermore, we show that the dynamic subcellular localization of LEFKOTHEA underpins its role in establishing a nucleus-chloroplast communication network that guides plant development.